The neurobiology of mammalian parenting and the biosocial context of human caregiving.

This article is part of a Special Issue "Parental Care". Research on the neurobiology of attachment, pioneered by scholars in the generation that followed the discovery of social bonding, examined the biological basis of mammalian parenting through systematic experiments in animal models and their application to theories on human attachment. This paper argues for the need to construct a theory on the neurobiology of human attachment that integrates findings in animal models with human neuroscience research to formulate concepts based on experimental, not only extrapolative data. Rosenblatt's (2003) three characteristics of mammalian parenting - rapid formation of attachment, behavioral synchrony, and mother-offspring attachment as basis of social organization - are used to guide discussion on mammalian-general versus human-specific attributes of parental care. These highlight specific components of attachment in rodents, primates, and humans that chart the evolution from promiscuous, nest-bound, olfactory-based bonds to exclusive, multi-sensory, and representation-based attachments. Following, three continua are outlined in parental behavior, hormones, and brain, each detailing the evolution from rodents to humans. Parental behavior is defined as a process of trophallaxis - the reciprocal multisensory exchange that supports approach orientation and enables collaboration in social species - and includes human-specific features that enable behavioral synchrony independent of tactile contact. The oxytocin system incorporates conserved and human-specific components and is marked by pulsatile activity and dendritic release that reorganize neural networks on the basis of species-specific attachment experiences. Finally, the subcortical limbic circuit underpinning mammalian mothering extends in humans to include multiple cortical networks implicated in empathy, mentalizing, and emotion regulation that enable flexible, goal-directed caregiving. I conclude by presenting a philosophical continuum from Hobbes to Lorenz, which illustrates how research on the neurobiology of attachment can put in the forefront the social-collaborative elements in human nature and afford a new perspective on the mind-brain polarity.